What Causes Population Cycles of Forest Lepidoptera?
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PERSPECTIVES to track numerical changes in their preyg. During the writing of this article, Werner What causes population cycles of forest Baltensweiler (Swiss Federal Institute of Technology, retired) sent me data on the Lepidoptera? two dominant parasitoids attacking the larch budmoth. Theoretical model-fitting (Box 1) indicates that the parasite-bud- Alan A. Berryman percapita rate of increase, R = ln(N,/N,-,), worm interaction only explains 28% of the and population density in the previous observed per-capita growth rate of the year, In N,-z, from which the effect of first- budworm and 50% of the parasitoids, Hypotheses for the causes of order correlation between R and In N,-, has which is hardly a dominant effect. regular cycles in populations of been removed. Lepidoptera with cyclical There seems to be little doubt, how- forest Lepidoptera have invoked dynamics are dominated by second-order ever, that population cycles of some for- pathogen-insect or foliage-insect feedback (PC2 > Kl) (see Fig. 1) while est Lepidoptera are the result of interac- interactions. However, the available those with more stable dynamics are domi- tions with insect parasitoids. For example, data suggest that forest caterpillar nated by first-order feedback (PC2 <Xl). Morris6 presented 11 years of data on the cycles are more likely to be the result The search for a general explanation density of blackheaded budworm (Acleris of interactions with insect parasitoids, for population cycles in forest Lepidop- UQriQnQ) caterpillars and their larval para- an old argument that seems to have tera has been approached from two major sitoids and concluded that the dynamics been neglected in recent years. directionsls. First, because of early preoccu- of the budworm were determined to a Aian Berryman is at the Depts of pations with direct causal processes, re- large degree by interaction with parasit- Entomology and Natural Resource Sciences, lationships were sought to external forces oids. Although McNamee31 has proposed Washington State University, Pullman, like climatic or sunspot cycles. This ap- an alternative explanation for blackheaded WA 99 164, USA. proach generally proved unfruitful be- budworm cycles, Morris’ conclusions have cause no external forces have been found been strongly supported by recent analy- to be strongly correlated with the rigid ses5.2s129.It is important to realize that any forest Lepidoptera exhibit re- periodicity seen in lepidopteran cycles. blackheaded budworm populations de- M markable variations in abundance, However, external forces are probably in- cline before food shortage becomes an often with almost clockwork regularity. volved in the synchronization of cycles important factor6J0, while larch budmoth Perhaps the most remarkable, and cer- over large geographic regionG24, and in declines are almost always associated with tainly the best documented, is the larch their persistence through timezs. heavy host-defoliation. In addition, theo- budmoth (Zeiraphera diniana), which goes The second approach involves circu- retical model-fitting (Box 1) indicates that, through lOOOO-foldchanges in density dur- lar causality, or negative feedback, in one unlike the larch budmoth, most of the vari- ing its very regular [8.24 f 0.27 (SE) years] form or another. Hutchinson seems to ation in observed blackheaded budworm cycle in the Alps (Fig. 1). But the time have been the first to recognize that cir- and parasitoid per-capita rates of change series in Fig. 1 also show that many forest cular causal processes in ecosystems can are explained by their mutual interaction caterpillars fluctuate with much less vari- give rise to delayed negative feedback that (76% and 91%, respectivelyzg). ability and regularity - cyciicity seems to can then induce cyclical dynamics in the Another case where parasitoids seem be common in the species we call ‘pests’ ecosystem variables (e.g. population den- to be involved is the spruce needleminer but it is definitely not the norm. It is also sities). Some claim that this is the only (Epinotia tedekz). Miinster-Swendsenn pre interesting to note that one of the defoli- truly general explanation for regular cycles sented a 20-year time series of the needle- ators in Fig. 1, the autumnal moth (Epirrita in animal populationsaJ7. Others, however, miner and its larval parasitoids inhabiting QQ~MTZ~Q~Q), is quite stable in the Alps (Fig. have proposed more-restrictive general a Norway spruce (Picea a&es) plantation lc) but exhibits cycles of similar amplitude explanations for lepidopteran cycles, by in Denmark, and used these data to con- and period to the larch budmoth in the hypothesizing that the negative feedback struct a detailed simulation model of the birch forests of northern Fennoscandiax. is the result of a particular biological interactions between needleminer, host Obviously, the occurrence of large-ampli- mechanism. Myers’s reviewed some of tree, parasitoids, predators, diseases and tude cycles in forest Lepidoptera also de- these hypotheses, but new data and recent weatherid. This model faithfully recreated pends on the environment in which the developments in ecological theory and the cyclical dynamics observed in this species lives. Cyclical dynamics seems to analysis provide a different perspective. and other plantations, leading Miinster- have more to do with the kind of ecological Swendsen to conclude that ‘parasitism is conditions to which the species is exposed Parasitoids the most important factor in limiting and than with the organism or its biological Despite the fact that early authors regulating the pest insect’. This conclu- attributess. found cause to link insect parasitoids to the sion was further supported by Berryman Be this as it may, the dynamics of many cyclic dynamics of certain forest Lepidop- and Miinster-SwendseG, who showed, forest Lepidoptera seem to be strongly tera637, this hypothesis has been largely by theoretical model-fitting, that 76% and affected by second-order feedback pro- overlooked in recent years. Yet, the foiiage- 81% of the variation in observed needle- cesse# or what is traditionally called feeding Lepidoptera are known to be at- miner and parasitoid per-capita rates of delayed density dependence6J (Table 1). tacked by numerous insect parasitoids in change, respectively, were explained by (‘Second order’ is a more informative term, the families Ichneumonidae, Braconidae, their mutual interaction. Like the biack- however, because it implies that the nega- Eulophidae and Chalcidae (Hymenoptera), headed budworm, the spruce needleminer tive feedback involves two mutually causal as well as Tachinidae and Sarcophagidae rarely causes severe defoliation to its host dynamic variables, such as predator-prey (Diptera). The larch budmoth, for example, tree. or plant-herbivore.) In Table 1, the relative is attacked by 94 species of parasitoidss. A third case is the gypsy moth (Lym- contribution of second-order feedback to However, parasitoids are not considered to antria dispar). Montgomery and Wallneril the observed dynamics is seen in K2, the be directly involved in the cyclical dynam- analyzed 26 years of data on the density of partial correlation between the observed ics of the budmoth but are thought merely the gypsy moth and its tachinid parasitoids 28 0 1996, Elsevier Science Ltd TREE vol. II, no. I January 1.996 PERSPECTIVES in former Yugoslavia (collected by P. Sisojevic, Institute for Biological Research, (4 (b) Beograd) and concluded that ‘the most ‘4i 101 plausible hypothesis is that specific tach- 12. inid parasitoids...are responsible for the 8- cyclical dynamics’. Turchins found signifi- x 10. .z2. cant second-order effects in the Yugoslav- .zEl 8. ii 6- ian gypsy moth time series (Table l), ; 6 0E 4- while theoretical model-fitting to the first 4~ 16 years of data (where second-order dy- 2. 2. namics dominate) indicates that the mu- tual interaction explains 71% and 75% of 0 0 the observed variation in the rates of 0 4 8 12 16 20 24 28 0 4 8 12 16 20 24 28 change of the gypsy moth and its parasit- Time Time oids, respectively. In addition, I have also found strong second-order effects in the (cl (4 North American gypsy moth series follow- ing its collapse from very high densities, and concluded that gypsy moth popu- lations had been controlled by introduced parasitoids33J4. In both North America and Yugoslavia, the gypsy moth occasion- ally causes severe defoliation of host trees but in a rather sporadic and inconsistent pattern in space and time. oi J 0- When data are available on both the 0 4 8 12 16 20 24 28 3 4 8 12 16 20 24 28 density of caterpillars and their parasit- Time Time oids over a number of years, they seem to support the hypothesis that population (e) cycles are often caused by interactions 6’ with insect parasitoids (in at least three out of four cases). But what of species for which there are insufficient published data? One way to approach this question is to compare parasitism rates in these species with those observed in the three dis- cussed above (Table 1). When we do this 1 we find that parasitism rates are consist- Oo i, -4 8 12 16 20 24 28> ently high in foliage-feeding caterpillars, usually exceeding all other causes of mor- Time tality and being more consistent during population declines. It is also important to Fig. 1. Population density fluctuations of Lepidoptera feeding on larch foliage in the Oberengadin Valley of realize that parasites can cause greater Switzerland. Data from Ref. 1 reported as the natural logarithm of numbers per 1000 kg of larch foliage. mortality than is apparent because they See text or Table 1 for definitions of PCl and PC2. (a) Zeiraphera diniana (Tortricidae); PC1 =-0.341, often feed on, sterilize or paralyze their PC2 = -0.788. (b) Exapate duratella (Tortricidae); PC1 = -0.388, PC2 =-0.594. (c) Epirrita autumnata (Geometridae); PC1 =-0.508, PC’2 =-0.276.